Immune-regulatory transcriptional responses in multiple organs of atlantic salmon after tributyltin exposure, alone or in combination with forskolin

Journal of Toxicology and Environmental Health - Part A: Current Issues

Volumn 74, Issue 7-9, 2011, Pages 478-493

  Pavlikova, Nela ^a,b   Arukwe, Augustine ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ALPHA INTERFERON; FORSKOLIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; MX3 PROTEIN; ORGANOTIN COMPOUND; PROTEIN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA; TRIBUTYLIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ATLANTIC SALMON; CONFERENCE PAPER; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOCOMPETENCE; IMMUNOREGULATION; JUVENILE; KIDNEY; LIVER; NONHUMAN; POLLUTANT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS;

ANIMALS; DISINFECTANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FORSKOLIN; GENE EXPRESSION; IMMUNE SYSTEM; INSULIN-LIKE GROWTH FACTOR I; INTERFERON-ALPHA; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-1BETA; KIDNEY; LIVER; RNA, MESSENGER; SALMO SALAR; TRANSFORMING GROWTH FACTOR BETA; TRIALKYLTIN COMPOUNDS; TUMOR NECROSIS FACTOR-ALPHA; WATER POLLUTANTS, CHEMICAL;

SALMO SALAR;

EID: 79952601616     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287394.2011.550558     Document Type: Conference Paper

References (91)

1. Akhurst, R. J., and Derynck, R. 2001. TGF-beta signaling in cancer\A double-edged sword. Trends Cell Biol. 11:S44-S51.
2. Allner, B., von der Gonna, S., Griebeler, E. M., Nikutowski, N., Weltin, A., and Stahlschmidt-Allner, P. 2010. Reproductive functions of wild fish as bioindicators of reproductive toxicants in the aquatic envi-ronment. Environ. Sci. Pollut. Res. 17: 505-518.
3. Arukwe, A. 2005. Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regula-tory (StAR) protein and cholesterol side chain cleavage (P450scc) in juvenile Atlantic salmon (Salmo salar) is a novel aspect of nonylphenol toxicity Environ. Sci. Technol. 39:9791-9798. (Pubitemid 41832163)
4. Atkins, C M., Oliva, A. A., Alonso, O. F., Pearse, D. D., Bramlett, H. M., and Dietrich, W D. 2007. Modulation of the cAMP signaling pathway after traumatic brain injury. Exp. Neurol. 208:145-158. (Pubitemid 47600157)
5. Bartee, E., Mohamed, M. R., and GMcFadden, G. 2008. Tumor necrosis factor and interferon: cytokines in harmony Curr. Opin. Microbiol. 11:378-383.
6. Bazzigher, L., Pavlovic, J., Haller, O., and Staeheli, P. 1992. Mxgenesshowweaker pri-mary response to virus than other interferon-regulated genes. Virology 186:154-160.
7. Belkowski, S. M., Rubin, C. S., and Prystowsky, M. B. 1998. Isolation and analysis of a T cell clone variant exhibiting constitutively phosphorylated Ser(133) cAMP response element-binding protein. J. Immunol. 161:659-665. (Pubitemid 28323527)
8. Berge, J. A., Brevik, E. M., Bjorge, A., Folsvik, N., Gabrielsen, G. W., and Wolkers, H. 2004. Organotins in marine mammals and seabirds from Norwegian territory.J. Environ. Monitor. 6:108-112. (Pubitemid 38299571)
9. Birchenough, A. C., Barnes, N., Evans, S. M., Hinz, H., Kronke, I., and Moss, C. 2002. A review and assessment of tributyltin contam-ination in the North Sea, based on surveys of butyltin tissue burdens and imposex/intersex in four species of neogastropods. Mar. Pollut. Bull. 44:534-543. (Pubitemid 34603708)
10. Campbell, B. K., Souza, C. J. H., Skinner, A. J., Webb, R., and Baird, D. T. 2006. Enhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein-2,-4, and-6. Endocrinology 147:1608-1620.
11. Carfi, M., Croera, C., Ferrario, D., Campi, V., Bowe, G., Pieters, R., and Gribaldo, L. 2008. TBTC induces adipocyte differentiation in human bone marrow long term culture. Toxicology 249:11-18.
12. Chen, T. C., Hinton, D. R., Zidovetzki, R., and Hofman, F M. 1998. Up-regulation of the cAMP/PKA pathway inhibits prolifera-tion, induces differentiation, and leads to apoptosis in malignant gliomas. Lab. Invest. 78:165-174. (Pubitemid 28113455)
13. Chesik, D., Wilczak, N., and De Keyser, J. 2008. IGF-1 regulates cAMP levels in astro-cytes through a beta2-adrenergic receptor-dependant mechanism. Int. J. Med. Sci. 5:240-243.
14. Clark, R. 1997. The somatogenic hormones and insulin-like growth factor-1: Stimulators of lymphopoiesis and immune function. Endocr. Rev. 18:157-179. (Pubitemid 27171518)
15. Corsini, E., Terzoli, A., Bruccoleri, A., Marinovich, M., and Galli, C L. 1997. Induction of tumor necrosis factor-alpha in vivo by a skin irritant, tributyltin, through activation of transcription factors: Its pharmacological modulation by anti-inflammatory drugs. J. Invest. Dermatol. 108:892-896. (Pubitemid 27272405)
16. Cuesta, A., Meseguer, J., and Esteban, M. A. 2008. Effects of the organochlorines p,p'-DDE and lindane on gilthead seabream leucocyte immune parameters and gene expression. Fish Shellfish Immunol. 25: 682-688.
17. Dinarello, C A. 1996. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147. (Pubitemid 26086851)
18. Duan, C M. 1998. Nutritional and devel-opmental regulation of insulin-like growth factors in fish.J. Nutr. 128:306S-314S.
19. Dudimah, F. D., Odman-Ghazi, S. O., Hatcher, F., and Whalen, M. M.2007. Effect of trib-utyltin (TBT) on ATP levels in human natural killer (NK) cells: Relationship to TBT-induced decreases in NK function. J. Appl. Toxicol. 27:86-94. (Pubitemid 46180790)
20. Eder, K. J., M. A. Clifford, R. P. Hedrick, H. R. Kohler, and I. Werner. 2008. Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pes-ticides and infectious hematopoietic necro-sis virus (IHNV). Fish Shellfish Immunol. 25:508-516.
21. Eder, K. J., Leutenegger, C. M., Wilson, B. W., and Werner, I. 2004. Molecularand cellular biomarker responses to pesticide exposure in juvenile chinook salmon (Oncorhynchus tshawytscha). Mar. Environ. Res.58:809-813. (Pubitemid 38738966)
22. Ekerbicer, N., Inan, S., Tarakci, F., and Zeren, T. 2009. The effects of DBcAMP on the expression of eNOS, iNOS and TGF-beta in rat heart tissue. Biotech. Histochem. 84: 47-54.
23. Ellis, D. V., and Pattisina, L. A. 1990. Widespread neogastropod imposex-a bio-logical indicator of global Tbt contamination. Mar. Pollut. Bull. 21:248-253.
24. Frouin, H., Lebeuf, M., Saint-Louis, R., Hammill, M., Pelletier, E., and M. Fournier, M. 2008. Toxic effects of tributyltin and its metabolites on harbour seal (Phoca vit-ulina) immune cells in vitro. Aquat. Toxicol. 90:243-251.
25. Ghoneum, M., Hussein, A. E., Gill, G., and Alfred, L. J. 1990. Suppression of murine natural-killer-cell activity by tributyltin\In vivo and in vitro assessment. Environ. Res. 52:178-186. (Pubitemid 20313146)
26. Gipperth, L. 2009. The legal design of the inter-national and European Union ban on trib-utyltin antifouling paint: Direct and indirect effects. J. Environ. Manage. 90:S86-S95.
27. Grivennikov, S. I., Greten, F. R., and Karin, M. 2010. Immunity inflammation, and cancer. Cell140:883-899.
28. Haddad, J. J., and Fahlman, C. S. 2002. Redox-and oxidant-mediated regulation of interleukin-10: An anti-inflammatory antioxidant cytokine? Biochem. Biophys. Res. Commun. 297:163-176. (Pubitemid 35216150)
29. Hammerman, M. R. 1999. The growth hormone-insulin-like growth factor axis in kidney re-revisited. Nephrol. Dialysis Transplant. 14:1853-1860. (Pubitemid 29358879)
30. Harford, A. J., O'Halloran, K., and Wright, P. F. A. 2007. Effect of in vitro and in vivo organotin exposures on the immune func-tions of murray cod (Maccullochella peelii peelii). Environ. Toxicol. Chem. 26:1649-1656. (Pubitemid 47265507)
31. Hasko, G., and Cronstein, B. N. 2004. Adenosine: An endogenous regulator of innate immunity. Trends Immunol. 25: 33-39. (Pubitemid 38032805)
32. Hasko, G., Szabo, C., Nemeth, Z. H., Kvetan, V., Pastores, S. M., and Vizi, E. S. 1996. Adenosine receptor agonists differentially regulate IL-10, TNF-alpha and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J. Immunol. 157:4634-4640. (Pubitemid 126449386)
33. Heemskerk, V H., Daemen, M., and Buurman, W. A. 1999. Insulin-like growth factor-1 (IGF-1) and growth hormone (GH) in immunity and inflammation. Cytokine Growth Factor Rev. 10:5-14. (Pubitemid 29230848)
34. Holzinger, D., Jorns, C., Stertz, S., Boisson-Dupuis, S., Thimme, R., Weidmann, M., Casanova, J. L., Haller, O.,and Kochs, G. 2007. Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling.J. Virol. 81:7776-7785. (Pubitemid 47047864)
35. Hong, S., Zou, J., Crampe, M., Peddie, S., Scapigliati, G., Bols, N., Cunningham, C., and Secombes, C J. 2001. The pro-duction and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1 beta. Vet. Immunol. Immunopathol. 81: 1-14. (Pubitemid 32717561)
36. Horiguchi, T., Shiraishi, H., Shimizu, M., and Morita, M. 1994. Imposex and organotin compounds in Thais clavigera and T. Bronni in Japan.J. Mar. Biol. Ass. UK 74:651-669. (Pubitemid 2110587)
37. Ingerslev, H. C., Cunningham, C., and Wergeland, H. I., 2006. Cloningand expres-sion of TNF-alpha, IL-1 beta and COX-2 in an anadromous and landlocked strain of Atlantic salmon (Salmo salar L.) during the smolting period. Fish Shellfish Immunol. 20:450-461. (Pubitemid 41571243)
38. Iwamura, C., Aihara, M., Nakazawa, M., Takahashi, K., Yoshioka, N., Matsukura, S., Hirasawa, T., Minami, M., and Ikezawa, Z. 2006. Effects of tributyltin on the devel-opment of atopic dermatitis-like eruptions in DS-Nh mice. Int. Arch. Allergy Immunol. 141:337-345. (Pubitemid 44783904)
39. Jang, S. I., Hardie, L. J., and Secombes, C J. 1994. Effects of transforming growth-factor beta(1) on rainbow-trout Oncorhynchus-mykiss macrophage respiratory burstactivity. Dev. Comp. Immunol. 18:315-323. (Pubitemid 24328159)
40. Kagawa, H., en, K., Okuzawa, K., and Tanaka, H. 2003. Effects of luteinizing hormone and follicle-stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovar-ian follicles of red seabream, Pagrus major. Biol. Reprod. 68:1562-568. (Pubitemid 36519758)
41. Kagawa, H., Kobayashi, M., Hasegawa, Y., and Aida, K. 1994. Insulin and insulin-like growth-factor-I and growth-factor-II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen. Comp. Endocrinol. 95:293-300.
42. Kajiwara, N., Niimi, S., Watanabe, Ito, M., Y, Takahashi, S., Tanabe, S., Khuraskin, L. S., and Miyazaki, N. 2002. Organochlorine and organotin compounds in Caspian seals (Phoca caspica) collected during an unusual mortality event in the Caspian Sea in 2000. Environ. Pollut. 117:391-402. (Pubitemid 34142211)
43. Kannan, K., Guruge, K. S., Thomas, N. J., Tanabe, S., and Giesy, J. P. 1998. Butyltin residues in southern sea otters (Enhydra lutris nereis) found dead along California coastal waters. Environ. Sci. Technol. 32: 1169-1175. (Pubitemid 28208678)
44. Kato, T., Tada-Oikawa, S., Takahashi, K., Saito, K., Wang, L., Nishio, A., Hakamada-Taguchi, R., Kawanishi, S., and Kuribayashi, K. 2006. Endocrine disruptors that deplete glutathione levels in APC promote Th2 polarization in mice leadingto the exacerba-tion of airway inflammation. Eur. J. Immunol. 36:1199-1209.
45. Kato, T., Uchikawa, R., Yamada, M., Arizono, N., Oikawa, S., Kawanishi, S., Nishio, A., Nakase, H., and Uribayashi, K. 2004. Environmental pollutant tributyltin pro-motes Th2 polarization and exacerbates air-way inflammation. Eur. J. Immunol. 34: 1312-1321. (Pubitemid 39256010)
46. Kergosien, D. H., and Rice, C D. 1998. Macrophage secretory function is enhanced by low doses of tributyltin-oxide (TBTO), but not tributyltin-chloride (TBTCl). Arch. Environ. Contam. Toxicol. 34:223-228. (Pubitemid 28134373)
47. Lane, R., Ghazi, S. O., and Whalen, M. M. 2009. Increases in cytosolic calcium ion lev-els in human natural killer cells in response to butyltin exposure. Arch. Environ. Contam. Toxicol. 57:816-825.
48. Lappas, C M., Sullivan, G. W., and Linden, J. 2005. Adenosine A(2A) agonists in devel-opment for the treatment of inflammation. Expert Opin. Invest. Drugs 14:797-806. (Pubitemid 41030948)
49. Lehmann, J. M., McKee, D. D., Watson, M. A., Willson, T. M., Moore, J. T., and Kliewer, S. A. 1998. The human orphan nuclear receptor PXR is activated by compounds that regulate CYP3A4 gene expression and cause drug interactions.J. Clin. Invest. 102: 1016-1023. (Pubitemid 28419246)
50. Leong, J. A. C., Trobridge, G. D., Kim, C H. Y., Johnson, M., and Simon, B. 1998. Interferon-inducible Mx proteins in fish. Immunol. Rev. 166:349-363. (Pubitemid 29008495)
51. Liu, Y R., Ye, W L., Zeng, X. M., Ren, W H., Zhang, Y Q., and Mei, Y A. 2008. K+ chan-nels and the cAMP-PKA pathway modulate TGF-beta 1-incluced migration of rat vas-cular myofibroblasts. J. Cell. Physiol. 216: 835-843.
52. Lokman, P. M., George, K. A. N., Divers, S. L., Algie, M., and Young, G. 2007. 11-Ketotestosterone and IGF-1 increase the size of previtellogenic oocytes from shortfinned eel, Anguilla australis, in vitro. Reproduction 133:955-967. (Pubitemid 47162586)
53. Lorenz, J. J., Furdon, P. J., Taylor, J. D., Verghese, M. W., Chandra, G., Kost, T. A., Haneline, S. A., Roner, L. A., and Gray, J. G. 1995. A cyclic adenosine-3',5'-monophosphate sig-nal is required for the induction of Il-1-beta by Tnf-alpha in human monocytes. J. Immunol. 155:836-844.
54. Lv, X. F., Zhou, Q. F., Luo, W R., Cao, D. D., Jiang, G. B., and Deng, Y L. 2009. Interacting effects of tributyltin and 17 beta-estradiol in male Chinese loach (Misgumus anguillicaudatus). Environ. Toxicol. 24: 531-537.
55. Maestro, M. A., Planas, J. V., Moriyama, S., Gutierrez, J., Planas, J., and Swanson, P. 1997. Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by iso-lated follicular layers of the preovulatory coho salmon ovarian follicle. Gen. Comp. Endocrinol. 10:189-201. (Pubitemid 27218131)
56. Misumi, I., Yada, T., Leong, J. A. C., and Schreck, C. B. 2009. The effect of in vitro exposure to tributyltin on the immune com-petence of chinook salmon (Oncorhynchus tshawytscha) leukocytes. Arch. Environ. Contam. Toxicol. 56:229-237.
57. Moses, H. L., and Serra, R. 1996. Regulation of differentiation by TGF-beta. Curr. Opin. Genet. Dev. 6:581-586.
58. Nakata, H., Sakakibara, A., Kanoh, M., Kudo, S., Watanabe, H., Nagai, N., Miyazaki, N., Asano, Y., and Tanabe, S. 2002. Evaluation of mitogen-induced responses in marine mam-mal and human lymphocytes by in-vitro exposure of butyltins and non-ortho copla-nar PCBs. Environ. Pollut. 120245-253.
59. Naviglio, S., Spina, A., Marra, M., Sorrentino, A., Chiosi, E., Romano, M., Improta, S., Budillon, A., Illiano, G., Abbruzzese, A., and Caraglia, M. 2007. Adenylate cyclase/cAMP pathway downmodulation counteracts apoptosis induced by IFN-alpha in human epidermoid cancer cells. J. Interferon Cytokine Res. 27:129-136. (Pubitemid 46294435)
60. Negatu, Z., Hsiao, S. M., and Wallace, R. A. 1998. Effects of insulin-like growth factor-I on final oocyte maturation and steroid production in Fundulus heteroclitus. Fish Physiol. Biochem. 19:13-21. (Pubitemid 128512777)
61. Noble, P. W., Lake, F. R., Henson, P. M., and Riches, D. W H. 1993. Hyaluronate activation of Cd44 induces insulin-like growth factor-I expression by a tumor-necrosis-factor-alpha dependent mechanism in murine macrophages. J. Clin. Invest. 91:2368-2377. (Pubitemid 23182485)
62. Nygaard, R., Husgard, S., Sommer, A. I., Leong, J. A. C., and Robertsen, B. 2000. Induction of Mx protein by interferon and double-stranded RNA in salmonid cells. Fish Shellfish Immunol. 10:435-450.
63. Ohta, Y, Nakagawa, K., Imai, Y, Katagiri, T., Koike, T., and Takaoka, K. 2008. Cyclic AMP enhances smad-mediated BMP signal-ing through PKA-CREB pathway J. Bone Mineral Metab. 26:478-484.
64. Ohtaki, K., Aihara, M., Takahashi, H., Fujita, H., Takahashi, K., Funabashi, T., Hirasawa, T., and Ikezawa, Z. 2007. Effects of tributyltin on the emotional behavior of C57BL/6 mice and the development of atopic dermatitis-like lesions in DS-Nh mice.J. Dermatol. Sci. 47:209-216. (Pubitemid 47077893)
65. Parrizas, M., Saltiel, A. R., and LeRoith, D. 1997. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3'-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272: 154-161. (Pubitemid 27021138)
66. Pavlikova, N., Kortner, T. M., and Arukwe, A. 2010. Modulation of acute steroidogenesis, peroxisome proliferator-activated receptors and CYP3A/PXR in salmon interrenal tis-sues by tributyltin and the second messen-ger activator, forskolin. Chem. Biol. Interact. 185:119-127.
67. Pitossi, F., Blank, A., Schroder, A., Schwarz, A., Hussi, P., Schwemmle, M., Pavlovic, J., and Staeheli, P. 1993. A functional Gtp-binding motif is necessary for antiviral activity of Mx proteins. J. Virol. 67:6726-6732. (Pubitemid 23309141)
68. Petersen, S., and Gustavson, K. 2000. Direct toxic effects of TBT on natural enclosed phytoplankton at ambient TBT concentra-tions of coastal waters. Ecotoxicology 9: 273-285.
69. Presti, R. M., Popkin, D. L., Connick, M., Paetzold, S., and Virgin, H. W 2001. Novel cell type-specific antiviral mechanism of interferon gamma action in macrophages.J. Exp. Med. 193:483-496. (Pubitemid 32524479)
70. Randelli, E., Buonocore, F., and Scapigliati, G. 2008. Cell markers and determinants in fish immunology. Fish Shellfish Immunol. 25:326-340.
71. Rotchell, J. M., and Ostrander, G. K. 2003. Molecular markers of endocrine disruption in aquatic organisms. J. Toxicol. Environ. Health B 6:453-495. (Pubitemid 37083012)
72. Secombes, C. J., Bird, S., Cunningham, C., and Zou, J. 1999. Interleukin-1 in fish. Fish Shellfish Immunol. 9:335-343. (Pubitemid 129592927)
73. Shah, Y. M., Ma, X. C., Morimura, K., Kim, I., and Gonzalez, F J. 2007. Pregnane X receptoractivation ameliorates DSS-induced inflammatory bowel disease via inhibition of NF-kappa B target gene expression. Am. J. Physiol. Gastrointestinal Liver Physiol. 292:G1114-G1122. (Pubitemid 46557773)
74. Snoeij, N. J., Punt, P. M., Penninks, A. H., and Seinen, W 1986. Effects of tri-normal-butyltin chloride on energy metabolism, macromolecular synthesis, precursor uptake and cyclic-AMP production in isolated rat thymocytes. Biochim. Biophys. Acta 852:234-243. (Pubitemid 17229816)
75. Sommer, N., Loschmann, P. A., Northoff, G. H., Weller, M., Steinbrecher, A., Steinbach, J. P., Lichtenfels, R., Meyermann, R., Riethmuller, A., Fontana, A., Dichgans, J., and Martin, R. 1995. The antidepressant rolipram sup-presses cytokine production and prevents autoimmune encephalomyelitis. Nat. Med. 1:244-248.
76. Strand, J., and acobsen, J. A. 2005. Accumulation and trophic transfer of organotins in a marine food web from the Danish coastal waters. Sci. Total Environ. 350:72-85. (Pubitemid 41446357)
77. Takahashi, S., Le, L T. H., Saeki, H., Nakatani, N., Tanabe, S., Miyazaki, N., and Fujise, Y 2000. Accumulation of butyltin compounds and total tin in marine mammals. Water Sci. Technol. 42:97-108.
78. Tomiyama, K., Yamaguchi, A., Kuriyama, T., and Arakawa, Y 2009. Analysis of mecha-nisms of cell death of T-lymphocytes induced by organotin agents. J. Immunotoxicol. 6:184-193.
79. van Buul-Offers, S. C., and Kooijman, R. 1998. The role of growth hormone and insulin-like growth factors in the immune system. Cell. Mol. LifeSci. 54:1083-1094. (Pubitemid 28491017)
80. Wajant, H., Pfizenmaier, K., and Scheurich, P. 2003. Tumor necrosis factor signaling. Cell Death Different. 10:45-65. (Pubitemid 36511832)
81. Webb, J. G., Tan, Y., Jaffa, M. A., and Jaffa, A. A. 2010. Evidence for prostacyclin and cAMP upregulation by bradykinin and insulin-like growth factor 1 in vascular smooth mus-cle cells. J. Receptors Signal Transduct. 30: 61-71.
82. Weber, G. M., and Sullivan, C. V. 2000. Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidoge-nesis in striped bass, Morone saxatilis. Biol. Reproduct. 63:1049-1057.
83. Weber, G. M., and Sullivan, C. V. 2005. Insulin-like growth factor-1 induces oocyte maturational competence but not meiotic resumption in white bass (Morone chrysops) follicles in vitro: Evidence for rapid evolu-tion of insulin-like growth factor action. Biol. Reproduct. 72:1177-1186. (Pubitemid 40547982)
84. Whalen, M. M., Ghazi, S., Loganathan, B. G., and Hatcher, F 2002a. Expression of CD16, CD18 and CD56 in tributyltin-exposed human natural killer cells. Chem. Biol. Interact. 139:159-176. (Pubitemid 34131715)
85. Whalen, M. M., and Green, C B. 1998. Lysis-sensitive targets stimulate an elevation of cAMP in human natural killer cells. Immunology 93:415-420. (Pubitemid 28133618)
86. Whalen, M. M., Green, S. A., and Loganathan, B. G. 2002b. Brief butyltin exposure induces irreversible inhibition of the cytotoxic func-tion on human natural killer cells, in vitro. Environ. Res. 88:19-29. (Pubitemid 34136736)
87. Whalen, M. M., and Loganathan, B. G. 2001. Butyltin exposure causes a rapid decrease in cyclic AMP levels in human lymphocytes. Toxicol. Appl. Pharmacol. 171: 141-148. (Pubitemid 32217664)
88. Wilson, S., Dzon, L., Reed, A., Pruitt, M., and Whalen, M. M. 2004. Effects of in vitro exposure to low levels of organ-otin and carbarnate pesticides on human natural killer cell cytotoxic function. Environ. Toxicol.19:554-563. (Pubitemid 39552265)
89. Xing, D. M., and Bonanno, J. A. 2009. Effect of cAMP on TGF beta 1-induced corneal keratocyte-myofibroblast transfor-mation. Invest. Ophthalmol. Visual Sci. 50:626-633.
90. Zidek, Z. 1999. Adenosine-cyclic AMP path-ways and cytokine expression. Eur. Cytokine Network 10:319-328. (Pubitemid 29415384)
91. Zhou, C., Tabb, M. M., Nelson, E. L., Grun, F., Verma, S., Sadatrafiei, A., Lin, M., Mallick, S., Forman, B. M., Thummel, K. E., and Blumberg, B. 2006. Mutual repres-sion between steroid and xenobiotic recep-tor and NF-kappaB signaling pathways links xenobiotic metabolism and inflammation.J. Clin. Invest. 116:2280-2289. (Pubitemid 44162338)